This file is part of the following reference:

Goudberg, Nicole Joanna (1990) The feeding ecology of

three species of North Queensland Upland rainforest

ringtail possums, Hemibelideus lemuroides,

Pseudocheirus herbertensis and Pseudocheirus archeri

(marsupialia: petauridae). PhD thesis, James Cook

University.

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THE FEEDING ECOLOGY OF THREE SPECIES OF

NORTH QUEENSLAND UPLAND RAINFOREST RINGTAIL POSSUMS,

HEMIBELIDEUS LEMUROIDES, PSEUDOCHEIRUS HERBERTENSIS

AND PSEUDOCHEIRUS ARCHERI (MARSUPIALIA• PETAURIDAE)

Thesis submitted by

Nicole Joanna GOUDBERG B.Sc. (Hons.)

in June 1990

for the degree of Doctor of Philosophy in

the Department of Zoology at

James Cook University of North Queensland.

DECLARATION

I declare that this thesis is my own work and has not been submitted in any form for another degree or diploma at any university or other institution of tertiary education. Information derived from the published or unpublished work of others has been acknowledged in the text and a list of references is given.

Nicole J. Goudberg

June 1990

STATEMENT ON ACCESS

I, the undersigned, the author of this thesis, understand that the following restriction placed by me on access to this thesis will not extend beyond three years from the date on which the thesis is submitted to the University.

I wish to place restriction on access to this thesis as follows:

Access not to be permitted for a period of one year.

After this period has elapsed I understand that James Cook University of North Queensland will make it available for use within the University Library and, by microfilm or other photographic means, allow access to users in other approved libraries. All users consulting this thesis will have to sign the following statement:

In consulting this thesis I agree not to copy or closely paraphrase it in whole or in part without the written consent of the author; and to make proper written acknowledgement for any assistance which I have obtained from it.

Nicole J. Goudberg

June 1990.

Frontispiece: Climbing to catch possums in their dens. (Steve Williams photo).

ACKNOWLEDGEMENTS

This project was initially conceived following conversations with John Winter. I thank him, and also my supervisors Drs. G.E. Heinsohn and R.M. Murray, for valuable advice throughout the course of this project. John's help, both in the field and in discussions, is gratefully acknowledged. Sincere thanks are also due to Tony Irvine and Jeff Tracey who taught me botanical taxonomy from scratch with patience and good humour. For advice on numerical taxonomy I am indebted to Dr. Bill Williams; the Australian Institute of Marine Science kindly gave me access to their Numerical Taxonomy Package. Dr. Brian Green analysed my hard won blood samples and donated the tritiated water. Without his help I would not have attempted to measure field metabolic rates. Ken Nagy kindly allowed me to use several unpublished energetics equations. I would also like to thank Drs. George Heinsohn, John Winter, Rhondda Jones and especially Helene Marsh for help in beating the manuscript into shape; Tony Boniface and Claudia MacGrath for teaching me the necessary forage analyses and making my 6 months in the nutrition lab. an enjoyable experience. Claudia is especially thanked for analysing the nitrogen digests. The radio telemetry went smoothly thanks to the expertise of Reg Mercer and the staff of the electronics department.

To the numerous people who helped me in the field I give my thanks. Special thanks go to Tim Moore who taught me to climb; the JCUNQ rock climbing club and QNPWS for lending me extra gear; Les Moore and Steve Williams who helped with the climbing, the catching and the blood letting; Bill Laurance for teaching me heart puncture and remaining cheerful despite the 2am visits with possums in hand; and Keith Smith and family, the best possum catching team in Herberton.

That I survived the field work in almost continual rain, mud and leeches is due to the practical and moral support of Mac and Betty Harrison of Wondecla (suppliers of hot showers, battery charging facilities, wine and emergency vehicle repairs). I would have given up years ago but for their kindness.

I would also like to thank Prof. D.M. Stoddart and the zoology post graduates at University of Tasmania, and A/Prof. A.K. Lee and the zoology post graduates at Monash University for hospitality, and enlightening discussions during my visits to both those institutions.

For help with computing I am indebted to Geoff Draper, Jamie Oliver and the staff at the JCUNQ Computer Centre.

For much needed and valued assistance with the graphics I thank Marietta Thyssen; she did a great job.

This project was funded by a Commonwealth Postgraduate Award with extra financial support from James Cook University special research grants to Drs. G.E. Heinsohn and H. Marsh and supporting grants from the Ecological Society of Australia and the M.A. Ingram Trust.

ABSTRACT

The feeding behaviour of three species of upland rainforest ringtail

possums (Hemibelideus lemuroides, Pseudocheirus herbertensis and P.

archeri) was studied in the field for 30 months in 1982, 1983 and 1985.

They were found to be selective folivores, choosing diverse diets that

changed with the phenology of favoured food species. Mature leaves

constituted the bulk of the diet of P. archeri and H. lemuroides, while P.

herbertensis ate more young leaves. Tree species and seasonal food items

(young leaves, fruits, flowers) were not exploited in the same proportion

in which they occurred. Rather, condensed tannin and fibre content

determined whether they were included in the diet. Protein was not an

important correlate to species feeding preferences although P. herbertensis

selected a higher protein diet than the other species. H. lemuroides

selected for a low fibre diet, and P. archeri selected for high fibre.

Both P. herbertensis and P. archeri preferred to feed on continuously

leafing tree species. The diets of all three species became more

specialized during the more difficult dry season, and became increasingly

opportunistic during the wet season when there was more suitable food

available. Foods were partitioned almost completely at the species and item

levels. No interference competition for food between or within the three

possum species was ever observed.

The field energy requirements of P. herbertensis and H. lemuroides

were determined by the doubly labelled water method during September-

October 1985 (spring). Although both rainforest species have a similar food

intake, H. lemuroides uses more energy for free existence than P.

herbertensis, and obtains extra energy from a significantly higher quality

diet than P. herbertensis. Behavioural adaptations reduce the energy needs

of all three species.

ii

CONTENTS

ACKNOWLEDGEMENTS

ABSTRACT ii

LIST OF TABLES vi

LIST OF FIGURES viii

1 GENERAL INTRODUCTION 1

1.1 Foraging strategies 1 1.2 Leaves as a food source 3

1.2.1 Structural compounds 4 1.2.2 Secondary compounds 4 1.2.3 Nutrient content 7 1.2.4 Variability 7 1.2.5 Ephemerality 7

1.3 Digestion 9 1.4 The study 12

2 THE STUDY ANIMALS 13

2.1 Taxonomic relationships 13 2.2 Distribution 14 2.3 Background natural history 16

2.3.1 H. lemuroides 16 2.3.2 P. herbertensis 17 2.3.3 P. archeri 19

2.4 Previous studies 20

3 THE STUDY SITE 26

3.1 Location 26 3.2 Forest type 26 3.3 Temperature and rainfall 27

4 PHENOLOGY 32

4.1 Introduction 32 4.1.1 Leafing phenology 32 4.1.2 Flowering phenology 33 4.1.3 Fruiting phenology 34

4.2 Methods 35 4.3 Results 37

4.3.1 Leafing phenology 38 4.3.2 Flowering phenology 40 4.3.3 Fruiting phenology 41

4.4 Discussion 43 4.4.1 Leafing 43 4.4.2 Flowering 45 4.4.3 Fruiting 46

4.5 Summary 47

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5 DIET AND FOOD SELECTION 57

5 1 Introduction 57 5.1.1 The primate arboreal folivores 57 5.1.2 Marsupial arboreal folivores 60 5.1.3 General considerations 65

5 2 Methods 68 5.2.1 Duration of field work 68 5.2.2 Spotlighting techniques 68 5.2.3 Capture and marking of animals 70 5.2.4 Telemetry techniques 71 5.2.5 Statistical methods 73

5 3 Results 76 5.3.1 Dietary composition 77 5.3.2 Leafing and food preference 83 5.3.3 Dietetic diversity and homogeneity 85 5.3.4 Use of individual tree species 88 5.3.5 Dietary overlap between species 90 5.3.6 Seral partitioning 91 5.3.7 Feeding activity 92 5.3.8 Feeding heights 93

5.4 Discussion 94 5.4.1 Evaluating the foraging strategies 95 5.4.2 Competition 98

6

FOOD QUALITY 121

6.1 Introduction 121 6.1.1 Factors governing leaf choice 121 6.1.2 Adaptations to a folivorous diet 124

6.2 Methods 126 6.2.1 Analytical methods 127 6.2.2 Statistical methods 131

6.3 Results 131 6.3.1 Variability of leaf quality 132

6.3.2 Food quality & feeding preferences 133 6.3.3 Gut measurements 136

6.4 Discussion 136 6.4.1 Diet selection 136 6.4.2 Foraging strategies 139

6.4.3 Distribution of secondary compounds 140 6.4.4 Conclusions 141

7 ENERGETICS 149

7 1 Introduction 149 7.1.1 The doubly labelled water method 149 7.1.2 Field metabolic rate 150

7.2 Methods 151 7.2.1 Field methods 151 7.2.2 Laboratory methods 152 7.2.3 Equations 153

iv

1,2 Results 153 7.3.1 Free water availability 153 7.3.2 Field production of carbon dioxide 154 7.3.3 Water turnover in the field 154 7.3.4 Relationship between CO2 production

and water influx 155 7.3.5 Metabolic scope 156 7.3.6 Food consumption 156

7.4 Discussion 157 7.4.1 Carbon dioxide production 157 7.4.2 Basal metabolic rate 158 7.4.3 Field metabolic rate 159 7.4.4 Scope of metabolism 161 7.4.5 Water relations 161 7.4.6 Food consumption 163

7.5 Conclusions 164

8 ASSESSING THE POSSUM FORAGING STRATEGIES 170

8.1 Food selection y possums

171 8.2 Energetic considerations

173 8.3 Food procurement

175 8.4 Possum ecology: Implications for conservaton 177 8.5 The original hypotheses 179

REFERENCES

181

A List of families and species of plant observed at monthly intervals. 201

B Table 1 Relative densities of the common tree species and important food species at L.G.S.F. 204

Table 2 Feeding records for H. lemuroides, P. herbertensis and P. archeri. 205

APPENDIX

APPENDIX

APPENDIX C Members of the 21 groups of plants identified by cluster analysis. 208

APPENDIX D Table 1 Allelochemical content of leaves of selected species. 211

Table 2 Fibre fractions & crude protein of young and mature foliage. 212

Table 3 Water content & leaf toughness of young and mature foliage 214

Table 4 Ten most preferred food items ranked by number of feeding observations. 216

Table 5 Nutritional factors affecting ranking of food items in the diets of the three possum species. 217

LIST OF TABLES

Table

Page

2.1

Studies of arboreal folivores from the wet tropics of Australia. 22

2.2 Diets of P. herbertensis and P. archeri taken from the literature. 23

3.1 The twenty most common tree species in the study site. 29

4.1 Correlation between leaf flush in understorey and overstorey species and rainfall that fell in the same month and the previous month. 49

4.2 Periods of major leaf flush of core food species. 50

4.3 The time during which ripe fruit is available on individual overstorey and understorey tree at Longland's Gap State Forest. 51

5.1

The proportion of plant items in the diets of H. lemuroides, P. herbertensis and P. acheri. 101

5.2

Core food plants in the diets of H. lemuroides, P. herbertensis and P. archeri. 102

5.3

The proportion of young foliage from two core species (Flindersia brayleyana, Sloanea langii) in the diet of H. lemuroides. 103

5.4

Seasonality in frequency of feeding on core food species by H. lemuroides. 104

5.5

Non leaf items included in the diets of H. lemuroides, P. herbertensis and P. archeri. 105

5.6

The proportion (%) of young and matures age leaves in the diets of H. lemuroides, P. herbertensis and P. archeri. 106

5.7 Percentage of young leaf feeding records in the diet of H. lemuroides during flush periods compared with the overall proportion of young leaf feeding records for this species for the whole study. 107

5.8 Families of plants used for food by the three possum species. 108

vi

Table Page

5.9

Core food species shared by two or more possum species shown as number of feeding records. 109

5.10 The seral classification of core food plants eaten by the three possum species. 110

5.11 Number of plant species eaten and percent feeding time (in one night) of radio-tracked animals. 111

6.1 Comparison of nutritional factors between ten leaf items most preferred by each species and eight items never eaten. 142

6.2 The proportion of feeding observations from Type I and Type II foods. 143

6.3 A comparison of mean nutritional quality of the top four food items on which the species are most specialized, with the mean nutritional quality of the minor species in the diet. 144

6.4

Average lengths of parts of the digestive tract of adult specimens of the three species, in centimetres. 145

7.1

Assumptions made in measuring water and energy flux using the doubly labelled water method. 151

7.2

Metabolic rate and water turnover in free-living P. herbertensis and H. lemuroides in August/September at Longland's Gap State Forest. 165

7.3

Estimated food consumption and energy metabolism of free-living possums. 166

7.4

Comparison of metabolic rates of forest dwelling, arboreal marsupials. 167

7.5

Comparison of water turnover rates in forest dwelling marsupials. 168

7.6

Weight of pouch young and condition of lactating ringtail possums. 169

vii

LIST OF FIGURES

Figure Page

Frontispiece: Climbing to catch possums in their dens.

2.1 H. lemuroides, P. herbertensis and P. archeri. 24

3.1 Location of study site in Longlands Gap State Forest. 30

3.2 Temperature and rainfall records for Herberton, the nearest weather station to the study site. 31

4.1 Phenological grouping of 55 tree species based on leafing characteristics observed over 30 months. 53

4.2 Phenogical grouping of 55 tree species based on flowering characteristics observed over 30 months. 54

4.3 Leafing and major flush periods of understorey and overstorey tree. 55

4.4 Flowering phenology of understorey and overstorey species. 55

4.5 Extended and seasonally flowering species in the overstorey. 55

4.6 Extended and seasonally flowering species in the understorey. 55

4.7 Fruiting phenology of understorey and overstorey plant species. 55

4.8 Phenological grouping of 55 plant species based on fruiting characteristics observed over 30 months. 56

5.1 Number of days per month spent in the field during 1982, 1983 and 1985. Total number of feeding observations collected each month during 1982, 1983 and 1985. 112

5.2 Monthly number of feeding records of core food species collected for H. lemuroides during the study. 113

viii

Figure

Page

5.3

Monthly number of feeding records of core food species collected for P. herbertensis during the study. 114

5.4 Monthly number of feeding records of core food species collected for P. archeri during the study. 115

5.5 Dietary diversity and eveness indices for H. lemuroides. Dietary diversity and eveness indices for P. herbertensis. Dietary diversity and eveness indices for P. archeri. 116

5.6 Feeding electivities of the three possum species and relative densities of common tree species at Longland's Gap State Forest. 117

5.7 Activity schedules of H.lemuroides, P. herbertensis and P. archeri in the wet season and dry season. 118

5.8 Feeding heights in trees of H. lemuroides, P. herbertensis and P. archeri. 119

6.1 Dendrogram resulting from cluster analysis of nutrition data. 147

ix